Neural networks involved in artistic creativity

Creativity has been proposed to be either the result of solely right hemisphere processes or of interhemispheric interactions. Little information is available, however, concerning the neuronal foundations of creativity. In this study, we introduced a new artistic task, designing a new tool (a pen), which let us quantitatively evaluate creativity by three indices of originality. These scores were analyzed in combination with brain activities measured by functional magnetic resonance imaging (fMRI). The results were compared between subjects who had been formally trained in design (experts) and novice subjects. In the experts, creativity was quantitatively correlated with the degree of dominance of the right prefrontal cortex over that of the left, but not with that of the right or left prefrontal cortex alone. In contrast, in novice subjects, only a negative correlation with creativity was observed in the bilateral inferior parietal cortex. We introduced structure equation modeling to analyze the interactions among these four brain areas and originality indices. The results predicted that training exerts a direct effect on the left parietal cortex. Additionally, as a result of the indirect effects, the activity of the right prefrontal cortex was facilitated, and the left prefrontal and right parietal cortices were suppressed. Our results supported the hypothesis that training increases creativity via reorganized intercortical interactions. Human Brain Mapp 2009. © 2008 Wiley‐Liss, Inc.

[1]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[2]  A. McIntosh,et al.  Network interactions among limbic cortices, basal forebrain, and cerebellum differentiate a tone conditioned as a Pavlovian excitor or inhibitor: fluorodeoxyglucose mapping and covariance structural modeling. , 1994, Journal of neurophysiology.

[3]  K. Bollen A New Incremental Fit Index for General Structural Equation Models , 1989 .

[4]  I. M. Harris,et al.  Selective right parietal lobe activation during mental rotation: a parametric PET study. , 2000, Brain : a journal of neurology.

[5]  A. McIntosh,et al.  Functional network interactions between parallel auditory pathways during Pavlovian conditioned inhibition , 1995, Brain Research.

[6]  J E Bogen,et al.  The other side of the brain. 3. The corpus callosum and creativity. , 1969, Bulletin of the Los Angeles neurological societies.

[7]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[8]  A. Katz The Relationships between Creativity and Cerebral Hemisphericity for Creative Architects, Scientists, and Mathematicians , 1986 .

[9]  J P Guilford,et al.  Intelligence Has Three Facets , 1968, Science.

[10]  H. Petsche Approaches to verbal, visual and musical creativity by EEG coherence analysis. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[11]  Mark S. Cohen,et al.  Changes in cortical activity during mental rotation. A mapping study using functional MRI. , 1996, Brain : a journal of neurology.

[12]  H. Petsche,et al.  Shadows of artistry: cortical synchrony during perception and imagery of visual art. , 2002, Brain research. Cognitive brain research.

[13]  S V Pakhomov,et al.  PET study of brain maintenance of verbal creative activity. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[14]  Frank Puga,et al.  Functional networks underlying latent inhibition learning in the mouse brain , 2007, NeuroImage.

[15]  Ruth Ann Atchley,et al.  Cerebral Hemispheric Mechanisms Linking Ambiguous Word Meaning Retrieval and Creativity , 1999, Brain and Cognition.

[16]  H. Heinze,et al.  Cortical Activations during the Mental Rotation of Different Visual Objects , 2001, NeuroImage.

[17]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[18]  E. Koechlin,et al.  The Architecture of Cognitive Control in the Human Prefrontal Cortex , 2003, Science.

[19]  M. Petrides,et al.  Functional activation of the human brain during mental rotation , 1997, Neuropsychologia.

[20]  H. Gruber Cognitive Psychology, Scientific Creativity, and the Case Study Method , 1981 .

[21]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[22]  S. Petersen,et al.  Direct Comparison of Prefrontal Cortex Regions Engaged by Working and Long-Term Memory Tasks , 2001, NeuroImage.

[23]  K. Nakamura,et al.  Activation of the right inferior frontal cortex during assessment of facial emotion. , 1999, Journal of neurophysiology.

[24]  B L Miller,et al.  Emergence of artistic talent in frontotemporal dementia , 1998, Neurology.

[25]  R. Sternberg,et al.  The concept of creativity: Prospects and paradigms. , 1998 .

[26]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[27]  A. Neubauer,et al.  EEG alpha oscillations during the performance of verbal creativity tasks: differential effects of sex and verbal intelligence. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  H. Petsche,et al.  Drawing on mind's canvas: Differences in cortical integration patterns between artists and non‐artists , 2005, Human brain mapping.

[29]  Werner Lutzenberger,et al.  Enhanced dynamic complexity in the human EEG during creative thinking , 1996, Neuroscience Letters.

[30]  John S. Gero,et al.  Drawings and the design process , 1998 .

[31]  M. Reuter The Biological Basis of Creativity , 2007 .

[32]  John J. Foxe,et al.  A topography of executive functions and their interactions revealed by functional magnetic resonance imaging. , 2004, Brain research. Cognitive brain research.

[33]  D. Levine,et al.  A neuropsychological theory of positive affect and its influence on cognition. , 1999, Psychological review.

[34]  Ruth Seurinck,et al.  Trial pacing in mental rotation tasks , 2005, NeuroImage.

[35]  M. Boden Dimensions of creativity , 1996 .

[36]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[37]  Subhash Sharma,et al.  Sample Size Effects on Chi Square and Other Statistics Used in Evaluating Causal Models , 1982 .

[38]  M. Mendez Dementia as a window to the neurology of art. , 2004, Medical hypotheses.

[39]  Y. Finkelstein,et al.  Impulsive artistic creativity as a presentation of transient cognitive alterations. , 1991, Behavioral medicine.

[40]  Pui-Wa Lei,et al.  Evaluating estimation methods for ordinal data in structural equation modeling , 2009 .

[41]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[42]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[43]  E. Tulving,et al.  Network Analysis of Positron Emission Tomography Regional Cerebral Blood Flow Data: Ensemble Inhibition during Episodic Memory Retrieval , 1996, The Journal of Neuroscience.

[44]  K. Hoppe Hemispheric specialization and creativity. , 1988, The Psychiatric clinics of North America.

[45]  K. Boone,et al.  Functional correlates of musical and visual ability in frontotemporal dementia , 2000, British Journal of Psychiatry.

[46]  Y. Miyashita,et al.  Callosal window between prefrontal cortices: cognitive interaction to retrieve long-term memory. , 1998, Science.

[47]  A. Dietrich,et al.  The cognitive neuroscience of creativity , 2004, Psychonomic bulletin & review.

[48]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[49]  Martha Ann Bell,et al.  Two- and three-dimensional mental rotation tasks lead to different parietal laterality for men and women. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[50]  Danielle S. Bassett,et al.  A validated network of effective amygdala connectivity , 2007, NeuroImage.

[51]  Takashi Hanakawa,et al.  Neural correlates underlying mental calculation in abacus experts: a functional magnetic resonance imaging study , 2003, NeuroImage.

[52]  Leslie G. Ungerleider,et al.  Distributed Neural Systems for the Generation of Visual Images , 2000, Neuron.

[53]  Hiroyuki Okada,et al.  Neural substrates in judgment process while playing go: a comparison of amateurs with professionals. , 2005, Brain research. Cognitive brain research.

[54]  Karl J. Friston,et al.  Assessing interactions among neuronal systems using functional neuroimaging , 2000, Neural Networks.

[55]  F. Gonzalez-Lima,et al.  Structural equation modeling and its application to network analysis in functional brain imaging , 1994 .

[56]  J. Risberg,et al.  On the neurobiology of creativity. Differences in frontal activity between high and low creative subjects , 2000, Neuropsychologia.

[57]  Katya Rubia,et al.  Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection , 2003, NeuroImage.

[58]  Jon M Fincham,et al.  Distinct roles of the anterior cingulate and prefrontal cortex in the acquisition and performance of a cognitive skill , 2006, Proceedings of the National Academy of Sciences.

[59]  Colin Martindale,et al.  EEG alpha asymmetry and creativity , 1984 .

[60]  J. Grafman,et al.  Human prefrontal cortex: processing and representational perspectives , 2003, Nature Reviews Neuroscience.

[61]  P. Bentler,et al.  Fit indices in covariance structure modeling : Sensitivity to underparameterized model misspecification , 1998 .

[62]  R. J. Seitz,et al.  Visual cortex activation in kinesthetic guidance of reaching , 2007, Experimental Brain Research.

[63]  K. Yuan,et al.  Structural Equation Modeling with Small Samples: Test Statistics. , 1999, Multivariate behavioral research.

[64]  M. L. Pucak,et al.  Dendritic morphology of callosal and ipsilateral projection neurons in monkey prefrontal cortex , 2002, Neuroscience.

[65]  Scott Peltier,et al.  Connectivity exploration with structural equation modeling: an fMRI study of bimanual motor coordination , 2005, NeuroImage.

[66]  A. Roberts,et al.  Inhibitory control and affective processing in the prefrontal cortex: neuropsychological studies in the common marmoset. , 2000, Cerebral cortex.

[67]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[68]  Karl J. Friston,et al.  Where bottom-up meets top-down: neuronal interactions during perception and imagery. , 2004, Cerebral cortex.

[69]  B. Hennessey The Social Psychology of Creativity , 2003, Encyclopedia of Creativity, Invention, Innovation and Entrepreneurship.

[70]  H. Eysenck Creativity and Personality: Suggestions for a Theory , 1993 .

[71]  Steven M. Smith,et al.  Creativity And The Mind: Discovering The Genius Within , 1995 .

[72]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[73]  S. Sesack,et al.  Callosal terminals in the rat prefrontal cortex: Synaptic targets and association with GABA‐immunoreactive structures , 1998, Synapse.

[74]  E. Paul Torrance,et al.  Hemisphericity and Creative Functioning. , 1982 .

[75]  F. Gonzalez-Lima,et al.  Network model of fear extinction and renewal functional pathways , 2007, Neuroscience.

[76]  M. Csíkszentmihályi Creativity: Flow and the Psychology of Discovery and Invention , 1996 .

[77]  Blake W. Johnson,et al.  Non-identical neural mechanisms for two types of mental transformation: event-related potentials during mental rotation and mental paper folding , 2003, Neuropsychologia.

[78]  Virginia A. Mann,et al.  Right Hemisphere Specialization for Mental Rotation in Normals and Brain Damaged Subjects , 1990, Cortex.

[79]  Semir Zeki,et al.  Artistic Creativity and the Brain , 2001, Science.

[80]  Rosa Aurora Chávez-Eakle,et al.  Cerebral blood flow associated with creative performance: A comparative study , 2007, NeuroImage.

[81]  M. Petrides,et al.  Wisconsin Card Sorting Revisited: Distinct Neural Circuits Participating in Different Stages of the Task Identified by Event-Related Functional Magnetic Resonance Imaging , 2001, The Journal of Neuroscience.

[82]  Edward M. Bowden,et al.  Neural Activity When People Solve Verbal Problems with Insight , 2004, PLoS biology.